Adolescent binge ethanol treatment alters adult brain regional volumes, cortical extracellular matrix protein and behavioral flexibility

Pharmacology Biochemistry and Behavior

Volumn 116, Issue , 2014, Pages 142-151

  Coleman, Leon Garland ^a   Liu, Wen ^a   Oguz, Ipek ^a,b   Styner, Martin ^a,b   Crews, Fulton T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Brooks Computer Science Building   (United States)

Author keywords

Alcohol; Behavioral flexibility; Extracellular matrix; MRI; Neurocan; Underage drinking

Indexed keywords

ALCOHOL; BREVICAN; HYALURONAN BINDING PROTEIN; NEUROCAN; SCLEROPROTEIN; TENACIN C; UNCLASSIFIED DRUG; WISTERIA FLORIBUNDA AGGLUTININ;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADULT ANIMAL; ALCOHOL ABSTINENCE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANTERIOR COMMISSURE; ARTICLE; BINGE DRINKING; BRAIN CORTEX; BRAIN REGION; BRAIN SIZE; BRAIN STEM; BRAIN VENTRICLE; CAPSULA INTERNA; CAUDATE NUCLEUS; CENTRAL GRAY MATTER; CEREBELLUM; CONTROLLED STUDY; CORPUS CALLOSUM; FOREBRAIN; GLOBUS PALLIDUS; HIPPOCAMPAL FIMBRIA; HIPPOCAMPUS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INFERIOR COLLICULUS; LEARNING; LOCOMOTION; MALE; MAZE TEST; MESENCEPHALON; MOUSE; NEOCORTEX; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLFACTORY BULB; OPEN FIELD BEHAVIOR; ORBITAL CORTEX; PRIORITY JOURNAL; PUTAMEN; SUPERIOR COLLICULUS; THALAMUS; AGE; ANIMAL; BRAIN; C57BL MOUSE; DRINKING BEHAVIOR; DRUG EFFECTS; METABOLISM;

MUS;

AGE FACTORS; ALCOHOL DRINKING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; ETHANOL; EXTRACELLULAR MATRIX PROTEINS; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL;

EID: 84889990926     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2013.11.021     Document Type: Article

References (73)

1. H. Al-Saffar, K. Lewis, E. Liu, A. Schober, J.J. Corrigan, and K. Shibata Lipopolysaccharide-induced hypothermia and hypotension are associated with inflammatory signaling that is triggered outside the brain Brain Behav Immun 28 2013 188 195
2. K.A. Badanich, H.C. Becker, and J.J. Woodward Effects of chronic intermittent ethanol exposure on orbitofrontal and medial prefrontal cortex-dependent behaviors in mice Behav Neurosci 125 6 2011 879 891
3. A. Badea, G.A. Johnson, and R.W. Williams Genetic dissection of the mouse brain using high-field magnetic resonance microscopy Neuroimage 45 4 2009 1067 1079
4. C.E. Bandtlow, and D.R. Zimmermann Proteoglycans in the developing brain: new conceptual insights for old proteins Physiol Rev 80 4 2000 1267 1290
5. R. Basak, and R. Bandyopadhyay Encapsulation of hydrophobic drugs in Pluronic F127 micelles: effects of drug hydrophobicity, solution temperature, and pH Langmuir 29 13 2013 4350 4356
6. G.R. Breese, D.H. Overstreet, and D.J. Knapp Conceptual framework for the etiology of alcoholism: a "kindling"/stress hypothesis Psychopharmacology (Berl) 178 4 2005 367 380
7. J.L. Brigman, C. Graybeal, and A. Holmes Predictably irrational: assaying cognitive inflexibility in mouse models of schizophrenia Front Neurosci 4 2010
8. S.A. Brown, S.F. Tapert, E. Granholm, and D.C. Delis Neurocognitive functioning of adolescents: effects of protracted alcohol use Alcohol Clin Exp Res 24 2 2000 164 171
9. M.R. Celio, and I. Blumcke Perineuronal nets - a specialized form of extracellular matrix in the adult nervous system Brain Res Brain Res Rev 19 1 1994 128 145
10. M.R. Celio, R. Spreafico, S. De Biasi, and L. Vitellaro-Zuccarello Perineuronal nets: past and present Trends Neurosci 21 12 1998 510 515
11. L.G. Coleman Jr., L.F. Jarskog, S.S. Moy, and F.T. Crews Deficits in adult prefrontal cortex neurons and behavior following early post-natal NMDA antagonist treatment Pharmacol Biochem Behav 93 3 2009 322 330
12. L.G. Coleman Jr., J. He, J. Lee, M. Styner, and F.T. Crews Adolescent binge drinking alters adult brain neurotransmitter gene expression, behavior, brain regional volumes, and neurochemistry in mice Alcohol Clin Exp Res 35 4 2011 671 688
13. M.A. Collins, T.D. Corso, and E.J. Neafsey Neuronal degeneration in rat cerebrocortical and olfactory regions during subchronic "binge" intoxication with ethanol: possible explanation for olfactory deficits in alcoholics Alcohol Clin Exp Res 20 2 1996 284 292
14. C. Costa, R. Tortosa, A. Domenech, E. Vidal, M. Pumarola, and A. Bassols Mapping of aggrecan, hyaluronic acid, heparan sulphate proteoglycans and aquaporin 4 in the central nervous system of the mouse J Chem Neuroanat 33 3 2007 111 123
15. F.T. Crews, C.J. Braun, B. Hoplight, R.C. Switzer III, and D.J. Knapp Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats Alcohol Clin Exp Res 24 11 2000 1712 1723
16. F.T. Crews, K. Nixon, and M.E. Wilkie Exercise reverses ethanol inhibition of neural stem cell proliferation Alcohol 33 1 2004 63 71
17. F. Crews, J. He, and C. Hodge Adolescent cortical development: a critical period of vulnerability for addiction Pharmacol Biochem Behav 86 2 2007 189 199
18. A. Dityatev, C.I. Seidenbecher, and M. Schachner Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain Trends Neurosci 33 11 2010 503 512
19. C.L. Ehlers, J.R. Criado, D.N. Wills, W. Liu, and F.T. Crews Periadolescent ethanol exposure reduces adult forebrain ChAT + IR neurons: correlation with behavioral pathology Neuroscience 199 2011 333 345
20. J.J. Escobar-Chavez, M. Lopez-Cervantes, A. Naik, Y.N. Kalia, D. Quintanar-Guerrero, and A. Ganem-Quintanar Applications of thermo-reversible pluronic F-127 gels in pharmaceutical formulations J Pharm Pharm Sci 9 3 2006 339 358
21. M.C. Fabio, M.E. Nizhnikov, N.E. Spear, and R.M. Pautassi Binge ethanol intoxication heightens subsequent ethanol intake in adolescent, but not adult, rats Dev Psychobiol 2013 10.1002/dev.21101 (Epub ahead of print)
22. C.B. Fortier, E.M. Steffen, G. Lafleche, J.R. Venne, J.F. Disterhoft, and R.E. McGlinchey Delay discrimination and reversal eyeblink classical conditioning in abstinent chronic alcoholics Neuropsychology 22 2 2008 196 208
23. Franklin, and Paxinos The mouse brain in stereotaxic coordinates 2001
24. R. Frischknecht, M. Heine, D. Perrais, C.I. Seidenbecher, D. Choquet, and E.D. Gundelfinger Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity Nat Neurosci 12 7 2009 897 904
25. J.N. Giedd Structural magnetic resonance imaging of the adolescent brain Ann N Y Acad Sci 1021 2004 77 85
26. J.N. Giedd, J. Blumenthal, N.O. Jeffries, F.X. Castellanos, H. Liu, and A. Zijdenbos Brain development during childhood and adolescence: a longitudinal MRI study Nat Neurosci 2 10 1999 861 863
27. N. Gogolla, P. Caroni, A. Luthi, and C. Herry Perineuronal nets protect fear memories from erasure Science 325 5945 2009 1258 1261
28. N. Gogtay, J.N. Giedd, L. Lusk, K.M. Hayashi, D. Greenstein, and A.C. Vaituzis Dynamic mapping of human cortical development during childhood through early adulthood Proc Natl Acad Sci U S A 101 21 2004 8174 8179
29. G. Gong, L.B. Yuan, L. Hu, W. Wu, L. Yin, and J.L. Hou Glycyrrhizin attenuates rat ischemic spinal cord injury by suppressing inflammatory cytokines and HMGB1 Acta Pharmacol Sin 33 1 2012 11 18
30. E. Gruber, R.J. DiClemente, M.M. Anderson, and M. Lodico Early drinking onset and its association with alcohol use and problem behavior in late adolescence Prev Med 25 3 1996 293 300
31. E.D. Gundelfinger, R. Frischknecht, D. Choquet, and M. Heine Converting juvenile into adult plasticity: a role for the brain's extracellular matrix Eur J Neurosci 31 12 2010 2156 2165
32. K.L. Hanson, K.L. Medina, C.B. Padula, S.F. Tapert, and S.A. Brown Impact of adolescent alcohol and drug use on neuropsychological functioning in young adulthood: 10-year outcomes J Child Adolesc Subst Abuse 20 2 2011 135 154
33. D.W. He, and B. Lennox Cerebral beriberi (Wernicke's encephalopathy); review of 52 cases in a Singapore prisoner-of-war hospital Lancet 1 6436 1947 11 17
34. R. Hingson, and M. Winter Epidemiology and consequences of drinking and driving Alcohol Res Health 27 1 2003 63 78
35. E. Isenberg-Grzeda, H.E. Kutner, and S.E. Nicolson Wernicke-Korsakoff- syndrome: under-recognized and under-treated Psychosomatics 53 6 2012 507 516
36. L. Johnston, P. O'Malley, J. Bachman, and J.E. Schulenberg Monitoring the future: national survey results on drug use, 1975-2008 Seconday school students, 2008 vol. 1 2009 National Institute on Drug Abuse Bethesda, MD [xxxiv]
37. J.M. Juraska, and J.A. Markham The cellular basis for volume changes in the rat cortex during puberty: white and gray matter Ann N Y Acad Sci 1021 2004 431 435
38. R.K. Lenroot, and J.N. Giedd Brain development in children and adolescents: insights from anatomical magnetic resonance imaging Neurosci Biobehav Rev 30 6 2006 718 729
39. C.C. Leonardo, A.K. Eakin, J.M. Ajmo, and P.E. Gottschall Versican and brevican are expressed with distinct pathology in neonatal hypoxic-ischemic injury J Neurosci Res 86 5 2008 1106 1114
40. F. Lucantonio, T.A. Stalnaker, Y. Shaham, Y. Niv, and G. Schoenbaum The impact of orbitofrontal dysfunction on cocaine addiction Nat Neurosci 15 3 2012 358 366
41. K.L. Medina, T. McQueeny, B.J. Nagel, K.L. Hanson, A.D. Schweinsburg, and S.F. Tapert Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects Alcohol Clin Exp Res 32 3 2008 386 394
42. L.J. Murray, and C. Ranganath The dorsolateral prefrontal cortex contributes to successful relational memory encoding J Neurosci 27 20 2007 5515 5522
43. J.A. Obernier, A.M. White, H.S. Swartzwelder, and F.T. Crews Cognitive deficits and CNS damage after a 4-day binge ethanol exposure in rats Pharmacol Biochem Behav 72 3 2002 521 532
44. P.M. O'Malley, L.D. Johnston, and J.G. Bachman Alcohol use among adolescents Alcohol Health Res World 22 2 1998 85 93
45. Y. Ostby, C.K. Tamnes, A.M. Fjell, L.T. Westlye, P. Due-Tonnessen, and K.B. Walhovd Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years J Neurosci 29 38 2009 11772 11782
46. M. Pascual, A.M. Blanco, O. Cauli, J. Minarro, and C. Guerri Intermittent ethanol exposure induces inflammatory brain damage and causes long-term behavioural alterations in adolescent rats Eur J Neurosci 25 2 2007 541 550
47. T. Paus, A. Zijdenbos, K. Worsley, D.L. Collins, J. Blumenthal, and J.N. Giedd Structural maturation of neural pathways in children and adolescents: in vivo study Science 283 5409 1999 1908 1911
48. A. Pfefferbaum, K.O. Lim, J.E. Desmond, and E.V. Sullivan Thinning of the corpus callosum in older alcoholic men: a magnetic resonance imaging study Alcohol Clin Exp Res 20 1996 752 757
49. A. Pfefferbaum, E. Adalsteinsson, and E.V. Sullivan Dysmorphology and microstructural degradation of the corpus callosum: interaction of age and alcoholism Neurobiol Aging 27 7 2006 994 1009
50. L. Qin, J. He, R.N. Hanes, O. Pluzarev, J.S. Hong, and F.T. Crews Increased systemic and brain cytokine production and neuroinflammation by endotoxin following ethanol treatment J Neuroinflammation 5 2008 10
51. L. Qin, Y. Liu, J.S. Hong, and F.T. Crews NADPH oxidase and aging drive microglial activation, oxidative stress, and dopaminergic neurodegeneration following systemic LPS administration Glia 61 6 2013 855 868
52. U. Rauch Extracellular matrix components associated with remodeling processes in brain Cell Mol Life Sci 61 16 2004 2031 2045
53. J.S. Riceberg, and M.L. Shapiro Reward stability determines the contribution of orbitofrontal cortex to adaptive behavior J Neurosci 32 46 2012 16402 16409
54. G. Schoenbaum, M.R. Roesch, T.A. Stalnaker, and Y.K. Takahashi A new perspective on the role of the orbitofrontal cortex in adaptive behaviour Nat Rev Neurosci 10 12 2009 885 892
55. P.K. Sharma, and S.R. Bhatia Effect of anti-inflammatories on Pluronic F127: micellar assembly, gelation and partitioning Int J Pharm 278 2 2004 361 377
56. P. Shaw, D. Greenstein, J. Lerch, L. Clasen, R. Lenroot, and N. Gogtay Intellectual ability and cortical development in children and adolescents Nature 440 7084 2006 676 679
57. J. Silver, and J.H. Miller Regeneration beyond the glial scar Nat Rev Neurosci 5 2 2004 146 156
58. L.P. Spear The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 24 4 2000 417 463
59. Substance Abuse and Mental Health Services Administration (SAMSA) Results from the 2006 National Survey on Drug Use and Health: national findings (Office of Applied Studies, NSDUH Series H-32, DHHS Publication No. SMA 07-4293) 2007 [Rockville, MD]
60. S.F. Tapert, and S.A. Brown Substance dependence, family history of alcohol dependence and neuropsychological functioning in adolescence Addiction 95 7 2000 1043 1053
61. V.P. Torchilin Structure and design of polymeric surfactant-based drug delivery systems J Control Release 73 2-3 2001 137 172
62. A.J. Watson, J.F. Walker, G.H. Tomkin, M.M. Finn, and J.A. Keogh Acute Wernickes encephalopathy precipitated by glucose loading Ir J Med Sci 150 10 1981 301 303
63. H. Wechsler, G.W. Dowdall, A. Davenport, and S. Castillo Correlates of college student binge drinking Am J Public Health 85 7 1995 921 926
64. A.M. White, R.W. Hingson, I.J. Pan, and H.Y. Yi Hospitalizations for alcohol and drug overdoses in young adults ages 18-24 in the United States, 1999-2008: results from the Nationwide Inpatient Sample J Stud Alcohol Drugs 72 5 2011 774 786
65. H.R. White, N.R. Marmorstein, F.T. Crews, M.E. Bates, E.Y. Mun, and R. Loeber Associations between heavy drinking and changes in impulsive behavior among adolescent boys Alcohol Clin Exp Res 35 2 2011 295 303
66. B. Wood, J. Currie, and K. Breen Wernicke's encephalopathy in a metropolitan hospital. A prospective study of incidence, characteristics and outcome Med J Aust 144 1 1986 12 16
67. J.W. Wright, A.J. Masino, J.R. Reichert, G.D. Turner, S.E. Meighan, and P.C. Meighan Ethanol-induced impairment of spatial memory and brain matrix metalloproteinases Brain Res 963 1-2 2003 252 261
68. K.A. Young, L.A. Holcomb, W.L. Bonkale, P.B. Hicks, U. Yazdani, and D.C. German 5HTTLPR polymorphism and enlargement of the pulvinar: unlocking the backdoor to the limbic system Biol Psychiatry 61 6 2007 813 818
69. K.A. Young, W.L. Bonkale, L.A. Holcomb, P.B. Hicks, and D.C. German Major depression, 5HTTLPR genotype, suicide and antidepressant influences on thalamic volume Br J Psychiatry 192 4 2008 285 289
70. S. Zhu, W. Li, M.F. Ward, A.E. Sama, and H. Wang High mobility group box 1 protein as a potential drug target for infection- and injury-elicited inflammation Inflamm Allergy Drug Targets 9 1 2010 60 72
71. D.R. Zimmermann, and M.T. Dours-Zimmermann Extracellular matrix of the central nervous system: from neglect to challenge Histochem Cell Biol 130 4 2008 635 653
72. J. Zou, and F. Crews Induction of innate immune gene expression cascades in brain slice cultures by ethanol: key role of NF-kappaB and proinflammatory cytokines Alcohol Clin Exp Res 34 5 2010 777 789
73. J. Zou, and F.T. Crews Inflammasome-IL-1beta signaling mediates ethanol inhibition of hippocampal neurogenesis Front Neurosci 6 2012 77